Feeding ecology of a lesser‐known arboreal giant: Grizzled Giant Squirrel (Ratufa macroura), Southern Western Ghats, India

Abstract Animal dietary choices help us understand a species' feeding behaviour and are particularly relevant in conservation management. The aim of this study was to gather knowledge on dietary choices and the foraging behaviour of the Grizzled Giant Squirrel (Ratufa macroura) in Chinnar Wildlife Sanctuary, Southern Western Ghats, Kerala, India. The objectives were in particular to determine the food composition, seasonal fluctuations in food selection and feeding technique. Through an observational sampling method, focal animal sampling, the Grizzled Giant Squirrel in Chinnar Wildlife Sanctuary was found to feed on 30 plant species belonging to 18 families. The most used plant family was Fabaceae, with eight species, followed by Moraceae (four species) and Anacardiaceae (two species). The food species consumed included 22 trees, four climbers, one liana, one paraphyte, one shrub and one succulent species. The squirrel spent the most time feeding on Bauhinia racemosa (19.79%), followed by Tamarindus indica (14.08%) and Nothopegia beddomei (9.89%). The squirrel's diet choice was primarily influenced by the availability of food tree species and food resources rather than the season and nontree species were also found in the diet of Grizzled Giant Squirrel. Although the Grizzled Giant Squirrel exhibits some plasticity in its dietary choices, the available diversity of mature trees and plants as food sources appears to be important for its conservation in the fragmented riparian forest of the Western Ghats in Southern India.

their presence only in southeast Asia and serve as biological indicators of the habitat quality (Koprowski & Rajamani, 2008;Thorington & Cifelli, 1989).
Of the four giant arboreal squirrels belonging to the genus Ratufa, three are found in Indian landscapes, with Malabar Giant Squirrel (Ratufa indica) is endemic to the Indian subcontinent, the Malayan Giant Squirrel (Ratufa bicolor) is found in Northeast India and the Grizzled Giant Squirrel (Ratufa macroura) is endemic to Southern India and Sri Lanka (Menon, 2014).The Grizzled Giant Squirrel (hereafter GGS) is listed as a near-threatened species (IUCN, 2022) and has three subspecies of which India harbours only one, Ratufa macroura dandolena (Ellerman, 1961;Johnsingh & Nameer, 2015;Menon, 2014).Mainly because of the sparse distribution of its habitat in its areas of occurrences, it shows one of the most remarkable examples of isolated populations among arboreal mammals (IUCN, 2019;Molur et al., 2005;Ramachandran, 1993).Due to habitat loss and hunting in most of its range, the remaining population in India are more threatened than in Sri Lanka (Goonatilake, 2019).
Like most squirrels, it is primarily diurnal, but its highest activity has been observed in the early and late hours of the day (Paulraj, 1991).
In India, the Chinnar Wildlife Sanctuary in Kerala is home to the second largest population of GGS.The habitat of the animal is extremely unique and is confined primarily to a narrow stretch of riparian vegetation along the Chinnar and Pambar rivers and their major tributaries in the sanctuary (Ramachandran, 1993).Thus, the protection of these fragmented habitats is of prime importance for the conservation of the species.Habitat fragmentation, the main cause of the decline in arboreal giant squirrel populations, has become a hot subject among investigators and therefore studies on the population status of giant squirrels are extensive (Gurjar et al., 2013).In India, researchers contributed more to the population, distribution and ecology of R. indica compared with GGS (Ojha et al., 2023).Even though the GGS is the oldest recorded species of the genus Ratufa, dating back to 1769 (Ellerman et al., 1961), very little is known about its ecological aspects (Datta & Rajamani, 2015;Ojha et al., 2023).
Very little published information is available on the feeding ecology of this species, including one study reporting 21 tree species forming the GGS diet (Kumar et al., 2007).An additional effort is warranted to achieve better understanding on its interaction with the ecosystem and preferred plant species (Kissling et al., 2014;Koprowski & Rajamani, 2008).
The ecological niche of an animal in an ecosystem can be revealed by understanding its diet and feeding behaviour (Bookhout, 1994;Dell'Agnello et al., 2019).Nutrient and energy contents play a major role in the selection of foods that the squirrels eat (Gurnell, 1987).
Feeding of arboreal squirrels like GGS is confined to the middle canopy and very rarely the animal comes to the ground to feed on the scattered seeds or pursue other activities (Steele & Koprowski, 2003).

Studies done in Srivilliputhur Grizzled Squirrel Sanctuary in Tamil
Nadu, Southern India, showed that seeds and young fruits form the bulk of the GGS diet (Joshua, 1992).Based on a few literatures available on the feeding ecology of GGS, it is evident that it depends on available food resources in various sites of occurrence (Arya, 2018;Joshua, 1992;Kumar et al., 2007).Feeding techniques on a tree are related to the morphology and the mode of locomotion of the species (Clutton-Brock & Harvey, 1977).Even though the feeding techniques of R. indica are described, there is a lack of literature evidence for the GGS (Ramachandran, 1992).The availability of food in an area is vital in supporting a minimum viable population for the squirrel to thrive (Palmer & Koprowski, 2014).Mammalian population dynamics are greatly dependent on and influenced by food availability and diet (Chapman et al., 2015).Therefore, the activity and foraging behaviour of squirrels may also get influenced by the differences in food availability and quality among habitats (Koli et al., 2013) Squirrels were found to concentrate their activities in regions with abundant food resources and avoid areas with inferior food sources (Lurz et al., 2000).Thus, the knowledge about the food preferences and feeding behaviour specific to the scattered locations where the GGS present is vital for its conservation and management in the country.
To protect and improve the conservation measures directed to an animal, especially a habitat specialist like the GGS, a proper understanding of the habitat requirement is vital (Mills, 1992).Here, we focussed on the foraging ecology of the GGS, to identify the food species and seasonal variation in food choice, diet composition and feeding technique.The diet and feeding behaviour of the GGS is not well known so far; thus, it would help in making specific management prescriptions for protecting the near-threatened GGS in one of its prime refugia in India.

| Observation methods
The sites of the present study are in the riparian forests based on the knowledge of the occurrence of GGS in Chinnar Wildlife Sanctuary (Ramachandran, 1993; Figure 1).The information on the composition and seasonal variation in the GGS diet was collected through observational sampling.Focal animal sampling was used following Altmann (1974).Each encountered individual was followed, until it was out of sight and everything the animal did during the period was recorded.The individual-level identification was not possible because of the type of vegetation and lack of expertise to easily distinguish the individuals only by direct observation.Two people were in the field, and only one (the same person) collected the data throughout the study period to avoid personal biases.Observation on the time spent on feeding, plant species eaten, plant part eaten, pickup rates of plant parts such as fruits, leaves, flowers, sap and bark were recorded.The data are structured as, encounters refer to how many times observer saw the squirrel (single individual or group entered as one encounter), and feeding incidences refers to number of feeding observations among all encounters.The feeding bouts mean the activities occur in bouts that are periods of, feeding activity within a food source or movement between two sources.The length of the bout was judged as the period between entry into and exit from a particular food source.During the period spent in the food source, some of the time was allotted to searching for a food item, selecting by smelling, remaining inactive or other grooming activities.The incidence of feeding on different food items across different seasons was categorised.This was done for three different seasons, summer (December-May), southwest monsoon (June-September) and northeast monsoon (October-November).
Observations were made for 10 months between April 2013 and May 2014, and within a month, at least 1 week was spent in the field.Five transects of 1000 m were laid after reconnaissance in the riparian habitat based on squirrel presence.Observations were made for each transect in both the forenoon and afternoon for an equal duration.Squirrels were observed using standard binoculars (model-8x40 S, Olympus Global, Tokyo, Japan).The identification of the plant species was done through collected samples and by direct observation using plant identification database (Sasidharan, 1999(Sasidharan, , 2010) ) Different feeding postures and feeding techniques used by the GGS were interpreted by direct observation during the sampling.

| Data analysis
To understand the diet composition of GGS, collected data were analysed by complementary approaches.The percentage contribution of different food items to the squirrel diet was calculated based on the duration of feeding on a particular item and the number of times of feeding incidence on a particular item.The Welch's t-test was used to test any significant difference in feeding bout and duration, in forenoon and afternoon hours.A circular analysis, Rayleigh test was done to check the association of a plant species fed by the GGS and seasons.A distance-based RDA analysis (similarity coefficient-Bray-Curtis) was done to depict the species usage by GGS against the seasons and time of the day as factors using Canoco5 (Braak & Smilauer, 2012;Legendre & Anderson, 1999).

| Food composition
The GGS was found to be feeding on different plant parts, including the leaves, seeds, flowers, sap and bark of different trees and other vegetation (Table 1).A total of 1314 min (in 10 months) in 42 encounters of feeding observation were collected during the study.
Feeding varied according to the availability of food in the different months.The GGS fed on Terminalia arjuna (January, April and September) and Tamarindus indica (May, November and December) in 3 different months, followed by Bauhinia racemosa (February and March), Ficus microcarpa (February and November) and Syzygium cumini (August, May) in 2 different months.However, the other species were observed to be eaten only once during the study period.
Climbing plants that were part of the diet included Derris brevipes, Diplocyclos palmatus and Cayratia trifolia.The GGS also used shrubs such as Hibiscus rosa-sinensis, cacti-Euphorbia trigona and liana-Entada rheedii as food.These species belong to 18 different families.
Among them, the preferred family was Fabaceae, with eight species, followed by Moraceae, with four species, and Anacardiaceae, with two species.

| Diurnal variation in feeding habit
The feeding duration recorded for the entire study period was 1314 min, including 915 feeding bouts.From the total feeding duration, 42% was recorded in the forenoon and the remaining 58% in the afternoon, with the sampling hours being the same for both times of day.During the morning feedings, 321 feeding bouts were counted, while in the afternoon approximately double was recorded with 594 bouts.However, the GGS were found to be inactive at a food source for some time before the start of the feeding or after feeding, before moving on to search for a new source or for other activities.In some cases, the GGS were found to be inactive or resting at a food source between periods of intensive feeding.The duration of feeding (t = 1.4649, p = .1524)and the feeding bout (t = 1.1923, p = .2424)between the forenoon and afternoon hours were found nonsignificant.

| Seasonal variation in diet
The frequency of feeding on all foods was highest in summer, followed by the northeast and southwest monsoons.Circular analysis showed that there was no concentration of data around a particular month of observation (p = .0843).Distance-based RDA revealed that the selection of plant species does not change systematically between seasons (and within a day).The GGS either choose the plant species at random or their choice is influenced by other aspects (e.g. when the fruits are ripe; Figure 3).

| Feeding technique
The GGS are very selective in their choice of food.Food selection seems to be based on odour (Figure 4a).The GGS were found to be handling its food with both mouth and forelimbs (Figure 4b).
Depending on the availability of food sources, the GGS moves to the top of the branch or other areas of the tree canopy and cuts the pod, fruit, leaves or flower with its mouth (Figure 4c).Occasionally, the food is brought to the mouth with the help of the forelimbs.With the fruit in its mouth, the squirrel then moves to the thick horizontal branch to latch on, sometimes feeding began at the point of harvest.
The squirrel holds the branch with the claws of the hind limbs and the hanging tail, which gives the body further balance (Figure 4d).
It then gnaws on the epicarp of the fruit to extract and consume the seed.During feeding, the forelimbs were effectively used to manipulate the food, be it long pods of Bauhinia racemosa or small fruits of Grewia tiliifolia.

| Feeding posture
Three main postures were observed in the present study.The most common feeding posture is that of the squirrel sitting on a horizontal branch of the tree and eating and the second posture is that of the animal hanging upside down on small branches, supporting itself with its hind limbs and tail, reaching for the food in the hanging TA B L E 1 Details of each feeding incident of the Grizzled Giant Squirrel on a particular species.posture.In the third feeding posture, the squirrel holds on the bole of the tree and eats upside down.
In most observations of feeding posture, it was found that squirrels eat sitting on the branch, holding the branch with their hind legs and their tail hanging down.The hanging tail helps the animal to balance its body.This type of posture was observed in feeding Bauhinia racemosa and Grewia tiliifolia (Figure 5a).The second posture consisted of GGS feeding hanging upside down from the branch using the claws of the hind legs, while the tail remained curled over the branch.This posture was mainly observed when feeding on fruit and flower clusters on small branches that could not support the squirrel's body weight.Sometimes this posture was also adopted just for harvesting.This was observed when GGS fed on Strychnos potatorum and Nothopegia beddomei (Figure 5b).
The third feeding posture observed was a GGS lying on the vertical bole, holding on to the bole with the claws of its hind legs and manipulating the food with its mouth and forelegs (Figure 5c).In the observed cases, the animals fed on the climbing plants they found on the trees or the tree sap and bark.

| DISCUSS ION
In the present study, GGS were found to feed on 30 different vegetation species including 22 tree species and eight species including climbers, lianas, paraphytes, shrubs and cacti in Chinnar Wildlife Sanctuary, Western Ghats, South India.Compared with an earlier report, in which 21 tree species were mentioned (Kumar et al., 2007), eight more species have been added.The GGS feed mainly on the seeds, tender leaves, flowers, bark and sap of these species, whereas in previous studies there was no mention of the GGS eating the plants or plant parts.The squirrels were observed to eat on tender leaves and flowers of plant species such as Derris brevipes and Diplocyclos palmatus (climbers), Entada rheedii (liana), Hibiscus rosa-sinensis (shrub) and Euphorbia trigona (cactus).In comparison with Joshua (1992) who reported that GGS fed on the tender leaves and flowers of two trees, Tamarindus indica and Bauhinia purpurea, our results showed that GGS fed extensively on the tender leaves of most of the tree species, which contributed to its diet.

| Food composition
The theory of optimal foraging proposed by Pyke (1984) states that a forager should only eat the most preferred or highest ranked item if a sufficient amount of that item is available to meet its daily nutritional requirements.When the preferred food item is exhausted, the forager should include the next highest-ranking item in its diet.
The percentage of different plant parts suggests that the GGS prefer more seeds in their diet and may switch more to leafy foods, flowers, sap and bark when seeds are scarce or unavailable.However, the present observation confirms the findings of (Thorington & Cifelli, 1989) on R. indica in Mudumalai Wildlife Sanctuary and (Ramachandran, 1992) in Periyar, Parambikulam and Silent Valley.
Thus, in the present study, we found that the GGS acts as an important seed disperser for many of the tree/plant species in the riverine vegetation.
F I G U R E 2 Contribution of each food item to total feeding based on (a) the duration of feeding on a particular item and (b) the number of times feeding on a particular item occurred.
F I G U R E 3 Distance-based redundancy analysis shows the association of season and time of day with the plant species fed by the Grizzled Giant Squirrel.The presence of the plant species in the diet was analysed against the seasons as one factor, northeast monsoon, southwest monsoon and summer (three levels) and time of the day as another factor, forenoon and afternoon (two levels).The distance matrix used was Bray-Curtis.
Rodents rely heavily on hoarding for their survival and reproduction (Vander Wall, 1990;Wang et al., 2018).In contrast to a report of hoarding by R. indica (Somanathan et al., 2007), there was no case of hoarding by GGS during the study period.This could either be a clear indication of optimal food availability in the habitat (Ando et al., 1985) or that GGS does not have this habit.Further studies on the energy budget of GGS are required, as this animal appears to be a plant generalist in this study area, feeding on seeds, leaves, flowers, sap and bark.

| Diurnal variation in feeding habit
The feeding observations over different hours of the day show that the animal was very active in the morning and evening hours of the day and rested during midday.The feeding activity thus seemed to be influenced by the weather factors in the region.In the hours when the sun was shining strongly or it was raining, the activity of the GGS was very low.Temperature-dependent activity patterns to avoid extreme weather conditions have already been observed in diurnal squirrels (Lee et al., 1990;Skibiel et al., 2002).

| Feeding posture and technique
The mouth and the forelimbs are the organs that help in handling the food, while the hind limbs and the tail serve as supporting organs for the balance of the body during feeding.It has been found that all three feeding postures, such as the sitting, hanging and clinging postures, are effectively utilised by the animal.This depends on the availability and type of food found.Similar feeding postures were reported by (Ramachandran, 1992) on Ratufa R. indica.Besides being the second largest GGS population in the country, Chinnar Wildlife Sanctuary has a very small piece of riparian habitat (1.6 km 2 ) that harbours a very small GGS population and is already under serious threat of habitat fragmentation and degradation (Thomas & Nameer, 2018).Further habitat fragmentation and degradation will lead to increased food scarcity and predation risk (Gurjar et al., 2013;Joshua & Johnsingh, 1994;Thomas et al., 2017).Food scarcity causes animals to increase the duration of food intake, which is positively correlated with stress (Dunn et al., 2010;Laurance et al., 2011).Habitat fragmentation accelerates the death of large and mature trees (Laurance et al., 2000), which has also been observed in the Chinnar Wildlife Sanctuary (Thomas

F
Feeding techniques: (a) selection by smell, (b) making the food reach to mouth with the help of forelimbs, (c) cutting the fruit with the mouth and (d) feeding the seeds by sitting on a firm branch.F I G U R E 5 Feeding postures: (a) sitting posture, (b) hanging posture and (c) clinging posture.